1232:, something fundamental for them to be able to fly, being transformed into a wing, or an antenna turning into a leg; in the mouse, two to four genes must be simultaneously removed to get a similar complete transformation. Some researchers believe that, because of the redundancy of the vertebrate HOX cluster plan and more constrained compared to invertebrate HOX clusters, the evolvability of vertebrate HOX clusters is, for some structural or functional reason, far lower than their invertebrate counterparts. This rapid evolvability is in part because invertebrates experienced much more dramatic episodes of
557:
at the bottom of such hierarchies to ultimately form the tissues, structures, and organs of each segment. Segmentation involves such processes as morphogenesis (differentiation of precursor cells into their terminal specialized cells), the tight association of groups of cells with similar fates, the sculpting of structures and segment boundaries via programmed cell death, and the movement of cells from where they are first born to where they will ultimately function, so it is not surprising that the target genes of Hox genes promote cell division, cell adhesion,
160:
203:. This implies that Hox genes arose over 550 million years ago. In bilateria, Hox genes are often arranged in gene clusters, although there are many exceptions where the genes have been separated by chromosomal rearrangements. Comparing homeodomain sequences between Hox proteins often reveals greater similarity between species than within a species; this observation led to the conclusion that Hox gene clusters evolved early in animal evolution from a single Hox gene via tandem
232:
528:
identify the set of proteins between two different species that are most likely to be most similar in function, classification schemes are used. For Hox proteins, three different classification schemes exist: phylogenetic inference based, synteny-based, and sequence similarity-based. The three classification schemes provide conflicting information for Hox proteins expressed in the middle of the body axis (
740:
actual functional sites. Especially for Hox proteins, which produce such dramatic changes in morphology when misexpressed, this raises the question of how each transcription factor can produce such specific and different outcomes if they all bind the same sequence. One mechanism that introduces greater DNA sequence specificity to Hox proteins is to bind protein cofactors. Two such Hox cofactors are
1212:, but the location is different. For example, there are more HOX genes on the 5' side of the mouse segment compared to the invertebrates. These genes correspond to expression in the tail, which would make sense as flies would not have anything similar to the tail that all vertebrates have. Additionally, in most vertebrates there are 39 members segregated into four separate tightly clustered
775:. For example, high concentrations of one maternal protein and low concentrations of others will turn on a specific set of gap or pair-rule genes. In flies, stripe 2 in the embryo is activated by the maternal proteins Bicoid and Hunchback, but repressed by the gap proteins Giant and Kruppel. Thus, stripe 2 will only form wherever there is Bicoid and Hunchback, but
412:
214:, Hox genes are expressed in staggered domains along the head-to-tail axis of the embryo, suggesting that their role in specifying position is a shared, ancient feature. The functional conservation of Hox proteins can be demonstrated by the fact that a fly can function to a large degree with a chicken Hox protein in place of its own. So, despite having a
862:
719:
terminal T being the most important for binding. This sequence is conserved in nearly all sites recognized by homeodomains, and probably distinguishes such locations as DNA binding sites. The base pairs following this initial sequence are used to distinguish between homeodomain proteins, all of which
556:
Hox genes act at many levels within developmental gene hierarchies: at the "executive" level they regulate genes that in turn regulate large networks of other genes (like the gene pathway that forms an appendage). They also directly regulate what are called realisator genes or effector genes that act
92:
sequence known as the homeobox, of which the term "Hox" was originally a contraction. However, in current usage the term Hox is no longer equivalent to homeobox, because Hox genes are not the only genes to possess a homeobox sequence; for instance, humans have over 200 homeobox genes, of which 39 are
57:
encode and specify the characteristics of 'position', ensuring that the correct structures form in the correct places of the body. For example, Hox genes in insects specify which appendages form on a segment (for example, legs, antennae, and wings in fruit flies), and Hox genes in vertebrates specify
832:
In some organisms, especially vertebrates, the various Hox genes are situated very close to one another on the chromosome in groups or clusters. The order of the genes on the chromosome is the same as the expression of the genes in the developing embryo, with the first gene being expressed in the
77:
An analogy for the Hox genes can be made to the role of a play director who calls which scene the actors should carry out next. If the play director calls the scenes in the wrong order, the overall play will be presented in the wrong order. Similarly, mutations in the Hox genes can result in body
61:
Studies on Hox genes in ciliated larvae have shown they are only expressed in future adult tissues. In larvae with gradual metamorphosis the Hox genes are activated in tissues of the larval body, generally in the trunk region, that will be maintained through metamorphosis. In larvae with complete
1421:
Hox genes play critical roles in the development of structures such as limbs, lungs, the nervous system, and eyes. As T. R. Lappin and colleagues observed in 2006, "Evolutionary conservation provides unlimited scope for experimental investigation of the functional control of the Hox gene network
1363:
The genetic studies by Morgan and others provided the foundation for the systematic analyses of Edward B. Lewis and Thomas
Kaufman, which provided preliminary definitions of the many homeotic genes of the Bithorax and Antennapedia complexes, and also showed that the mutant phenotypes for most of
527:
Proteins with a high degree of sequence similarity are also generally assumed to exhibit a high degree of functional similarity, i.e. Hox proteins with identical homeodomains are assumed to have identical DNA-binding properties (unless additional sequences are known to influence DNA-binding). To
1251:
In mouse embryos, the HOX10 genes, which is one of the genes that lie in the tail portion of the animal, turn the "rib-building" system off when the gene is activated. The genes are active in the lower back, where the vertebrae do not grow ribs, and inactive in the mid-back, allowing ribs to be
739:
However, all homeodomain-containing transcription factors bind essentially the same DNA sequence. The sequence bound by the homeodomain of a Hox protein is only six nucleotides long, and such a short sequence would be found at random many times throughout the genome, far more than the number of
817:
regulates differential expression of Hox genes along the anteroposterior axis. Genes in the 3' ends of Hox clusters are induced by retinoic acid resulting in expression domains that extend more anteriorly in the body compared to 5' Hox genes that are not induced by retinoic acid resulting in
843:
The Hox genes are named for the homeotic phenotypes that result when their function is disrupted, wherein one segment develops with the identity of another (e.g. legs where antennae should be). Hox genes in different phyla have been given different names, which has led to confusion about
148:
Helix 1 Helix 2 Helix 3/4 ______________ __________ _________________ RRRKRTAYTRYQLLELEKEFLFNRYLTRRRRIELAHSLNLTERHIKIWFQNRRMKWKKEN ....|....|....|....|....|....|....|....|....|....|....|....| 10 20 30 40 50
1256:
are experimentally inactivated, the vertebrae of the lower back grow ribs. This research prompted an evolutionary search for these mutations among all animals. An example of this is in lizards and snakes. In snakes, HOX10 genes have lost their rib-blocking ability in that way.
317:
gene was initially so named because it disrupted the labial appendage; however, the lab gene is not expressed in the labial segment, and the labial appendage phenotype is likely a result of the broad disorganization resulting from the failure of head involution.
768:. This results in a transcription factor cascade: maternal factors activate gap or pair-rule genes; gap and pair-rule genes activate Hox genes; then, finally, Hox genes activate realisator genes that cause the segments in the developing embryo to differentiate.
1187:
of the back, and the skeletal muscles of the body wall and limbs. HOX genes help differentiate somite cells into more specific identities and direct them to develop differently depending on where they are in the body. A large difference between vertebrates and
1174:
bodies are not segmented in the same way as insects; they are on average much more complex, leading to more infrastructure in their body plan compared to insects. HOX genes control the regulation and development of many key structures in the body, such as
1153:
which occurred in their evolutionary history. In zebrafish, one of the eight Hox gene clusters (a Hoxd cluster) has lost all protein-coding genes, and just a single microRNA gene marks the location of the original cluster. In some teleost fish, such as
124:
through which they either activate or repress hundreds of other genes. The same Hox protein can act as a repressor at one gene and an activator at another. The ability of Hox proteins to bind DNA is conferred by a part of the protein referred to as the
540:). A combined approach used phylogenetic inference-based information of the different species and plotted the protein sequence types onto the phylogenetic tree of the species. The approach identified the proteins that best represent ancestral forms (
833:
anterior end of the developing organism. The reason for this colinearity is not yet completely understood, but could be related to the activation of Hox genes in a temporal sequence by gradual unpacking of chromatin along a gene cluster.
438:
patterns T3 largely by repressing genes involved in wing formation. The wing blade is composed of two layers of cells that adhere tightly to one another, and are supplied with nutrient by several wing veins. One of the many genes that
4078:
Kulakova M, Bakalenko N, Novikova E, Cook CE, Eliseeva E, Steinmetz PR, et al. (January 2007). "Hox gene expression in larval development of the polychaetes Nereis virens and
Platynereis dumerilii (Annelida, Lophotrochozoa)".
97:
is the same as the order of their expression along the anterior-posterior axis of the developing animal, and are thus said to display colinearity. Production of Hox gene products at wrong location in the body is associated with
361:
in the embryo results in a failure of head involution (see labial gene), with a loss of larval head structures. Mutations in the adult have either deletions of parts of the head or transformations of head to thoracic identity.
720:
have similar recognition sites. For instance, the nucleotide following the TAAT sequence is recognized by the amino acid at position 9 of the homeodomain protein. In the maternal protein Bicoid, this position is occupied by
312:
embryo to internalize the mouth and head structures that initially develop on the outside of its body (a process called head involution). Failure of head involution disrupts or deletes the salivary glands and pharynx. The
2552:
Vachon G, Cohen B, Pfeifle C, McGuffin ME, Botas J, Cohen SM (October 1992). "Homeotic genes of the
Bithorax complex repress limb development in the abdomen of the Drosophila embryo through the target gene Distal-less".
848:
is made up of two clusters, the
Antennapedia complex and the Bithorax complex, which together were historically referred to as the HOM-C (for Homeotic Complex). Although historically HOM-C genes have referred to
247:
is an important model for understanding body plan generation and evolution. The general principles of Hox gene function and logic elucidated in flies will apply to all bilaterian organisms, including humans.
1195:
Due to the fact that the HOX genes are so highly conserved, most research has been done on much simpler model organisms, such as mice. One of the major differences that was noticed when comparing mice and
821:
Quantitative PCR has shown several trends regarding colinearity: the system is in equilibrium and the total number of transcripts depends on the number of genes present according to a linear relationship.
455:
is misexpressed in the second thoracic segment, such as occurs in flies with the "Cbx" enhancer mutation, it represses wing genes, and the wings develop as halteres, resulting in a four-haltered fly.
1360:). It transforms the third thoracic segment (T3) toward the second (T2). Bithorax arose spontaneously in the laboratory and has been maintained continuously as a laboratory stock ever since.
120:
The products of Hox genes are Hox proteins. Hox proteins are a subset of transcription factors, which are proteins that are capable of binding to specific nucleotide sequences on DNA called
1236:
and mutations. More than 20 major clades of invertebrates differ so radically in body organization, partly due to a higher mutation rate, that they became formally classified as different
1422:
which is providing important insights into human disease." In the future, more research can be done in investigating the roles of Hox genes in leukaemia and cancer (such as EOC).
252:, like all insects, has eight Hox genes. These are clustered into two complexes, both of which are located on chromosome 3. The Antennapedia complex (not to be confused with the
58:
the types and shape of vertebrae that will form. In segmented animals, Hox proteins thus confer segmental or positional identity, but do not form the actual segments themselves.
1352:
Definitive evidence for a genetic basis of some homeotic transformations was obtained by isolating homeotic mutants. The first homeotic mutant was found by Calvin
Bridges in
207:
and subsequent divergence, and that a prototypic Hox gene cluster containing at least seven different Hox genes was present in the common ancestor of all bilaterian animals.
785:
strands located in Hox clusters have been shown to inhibit more anterior hox genes ("posterior prevalence phenomenon"), possibly to better fine tune its expression pattern.
1446:
1349:'s genetic principles, Bateson and others realized that some examples of homeosis in floral organs and animal skeletons could be attributed to variation in genes.
145:
chain is shown below: Hox proteins often act in partnership with co-factors, such as PBC and Meis proteins encoded by very different types of homeobox gene.
408:
to be expressed in the antennal imaginal disc, so that, instead of forming an antenna, the disc makes a leg, resulting in a leg coming out of the fly's head.
1916:
de Rosa R, Grenier JK, Andreeva T, Cook CE, Adoutte A, Akam M, et al. (June 1999). "Hox genes in brachiopods and priapulids and protostome evolution".
4830:
744:(Exd) and Homothorax (Hth). Exd and Hth bind to Hox proteins and appear to induce conformational changes in the Hox protein that increase its specificity.
78:
parts and limbs in the wrong place along the body. Like a play director, the Hox genes do not act in the play or participate in limb formation themselves.
1125:
to give four Hox gene clusters: Hoxa, Hoxb, Hoxc and Hoxd. It is currently unclear whether these duplications occurred before or after the divergence of
218:
that lived over 550 million years ago, the chicken and fly version of the same Hox gene are similar enough to target the same downstream genes in flies.
2510:"Analysis of central Hox protein types across bilaterian clades: on the diversification of central Hox proteins from an Antennapedia/Hox7-like protein"
4820:
853:
homologues, while Hox genes referred to vertebrate homologues, this distinction is no longer made, and both HOM-C and Hox genes are called Hox genes.
1192:
is the location and layering of HOX genes. The fundamental mechanisms of development are strongly conserved among vertebrates from fish to mammals.
3543:"Enigmatic orthology relationships between Hox clusters of the African butterfly fish and other teleosts following ancient whole-genome duplication"
1158:, an even more recent genome duplication occurred, doubling the seven or eight Hox gene clusters to give at least 13 clusters Another teleost, the
2136:"Rescue of Drosophila labial null mutant by the chicken ortholog Hoxb-1 demonstrates that the function of Hox genes is phylogenetically conserved"
2353:"The homeotic gene Sex combs reduced of Drosophila melanogaster is differentially regulated in the embryonic and imaginal stages of development"
434:
The third thoracic segment, or T3, bears a pair of legs and a pair of halteres (highly reduced wings that function in balancing during flight).
4798:
4274:
2878:
1383:
93:
Hox genes. Hox genes are thus a subset of the homeobox transcription factor genes. In many animals, the organization of the Hox genes in the
1436:
1166:
443:
represses is blistered, which activates proteins involved in cell-cell adhesion, and spalt, which patterns the placement of wing veins. In
62:
metamorphosis the Hox genes are mainly expressed in juvenile rudiments and are absent in the transient larval tissues. The larvae of the
4763:
2599:
Capovilla M, Botas J (December 1998). "Functional dominance among Hox genes: repression dominates activation in the regulation of Dpp".
4336:
4608:
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2733:
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identified and classified 15 genes of key importance in determining the body plan and the formation of body segments of the fruit fly
716:
42:
4308:
2745:
1410:
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no longer represses wing genes, and the halteres develop as a second pair of wings, resulting in the famous four-winged flies. When
4351:
4346:
487:
is ectopically expressed throughout the embryo, all segments anterior of A4 are transformed to an A4-like abdominal identity. The
4565:
4122:
Lee PN, Callaerts P, De Couet HG, Martindale MQ (August 2003). "Cephalopod Hox genes and the origin of morphological novelties".
548:) and the proteins that represent new, derived versions (or were lost in an ancestor and are now missing in numerous species).
736:. If the lysine in Bicoid is replaced by glutamine, the resulting protein will recognize Antennapedia-binding enhancer sites.
396:
gene specifies this identity by promoting leg formation and allowing (but not directly activating) wing formation. A dominant
4742:
1371:
353:
gene is responsible for the formation of the maxillary and mandibular segments in the larval head. The mutant phenotypes of
4593:
3408:"Comparative phylogenomic analyses of teleost fish Hox gene clusters: lessons from the cichlid fish Astatotilapia burtoni"
1121:
The ancestors of vertebrates had a single Hox gene cluster, which was duplicated (twice) early in vertebrate evolution by
4560:
519:
abdomen. Both the regulatory protein and the morphogenic protein are involved in the development of the tail segment.
215:
3674:
Daniels LK (January 1976). "Rapid in-office and in-vivo desensitization of an injection phobia utilizing hypnosis".
4752:
4618:
4450:
2810:
Hanes SD, Brent R (January 1991). "A genetic model for interaction of the homeodomain recognition helix with DNA".
1972:"Pre-bilaterian origins of the Hox cluster and the Hox code: evidence from the sea anemone, Nematostella vectensis"
1390:
276:). The Bithorax complex, named after the Ultrabithorax gene, consists of the remaining three genes: Ultrabithorax (
3345:
Spagnuolo, A., Ristoratore, F., Di
Gregorio, A., Aniello, F., Branno, M. & Di Lauro, R. (2003) Gene 309, 71–79
2636:"The Drosophila Hox gene deformed sculpts head morphology via direct regulation of the apoptosis activator reaper"
4445:
4188:
Nüsslein-Volhard C, Wieschaus E (October 1980). "Mutations affecting segment number and polarity in
Drosophila".
1675:
Pearson JC, Lemons D, McGinnis W (December 2005). "Modulating Hox gene functions during animal body patterning".
1356:'s laboratory in 1915. This mutant shows a partial duplication of the thorax and was therefore named Bithorax (
1159:
1122:
483:
loss-of-function mutants, abdominal segments A2 through A8 are transformed into an identity more like A1. When
1248:
changes for the most part. This is also one reason why homeotic mutations in vertebrates are so rarely seen.
3960:"Evolution of Antp-class genes and differential expression of Hydra Hox/paraHox genes in anterior patterning"
3057:
Fraser P, Bickmore W (May 2007). "Nuclear organization of the genome and the potential for gene regulation".
4686:
4623:
4598:
4481:
4401:
3357:"A new look at an old question: when did the second whole genome duplication occur in vertebrate evolution?"
796:
327:
243:
3457:
Woltering JM, Durston AJ (June 2006). "The zebrafish hoxDb cluster has been reduced to a single microRNA".
3295:
Garcia-Fernández J, Holland PW (August 1994). "Archetypal organization of the amphioxus Hox gene cluster".
2304:"Developmental and molecular analysis of Deformed; a homeotic gene controlling Drosophila head development"
159:
4825:
4671:
4570:
4555:
4524:
4425:
2763:"DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9"
1306:
1290:
791:(ncRNA) has been shown to be abundant in Hox clusters. In humans, 231 ncRNA may be present. One of these,
301:
103:
795:, silences in trans (it is transcribed from the HOXC cluster and inhibits late HOXD genes) by binding to
304:(an appendageless segment between the antenna and mandible), and also in the midgut. Loss of function of
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4603:
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4435:
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4301:
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Holland LZ, Albalat R, Azumi K, Benito-Gutiérrez E, Blow MJ, Bronner-Fraser M, et al. (July 2008).
401:
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Just as Hox genes regulate realisator genes, they are in turn regulated themselves by other genes. In
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4534:
4529:
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4393:
4197:
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3066:
2819:
2462:
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1983:
1925:
1839:
1785:
1730:
1479:
807:
82:
3159:"Modeling Hox gene regulation in digits: reverse collinearity and the molecular origin of thumbness"
4787:
3010:"Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs"
1402:
772:
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is transcribed in two different forms, a regulatory protein, and a morphogenic protein. Regulatory
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The DNA sequence bound by the homeodomain protein contains the nucleotide sequence TAAT, with the
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86:
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Lempradl A, Ringrose L (February 2008). "How does noncoding transcription regulate Hox genes?".
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2011:
1970:
Ryan JF, Mazza ME, Pang K, Matus DQ, Baxevanis AD, Martindale MQ, et al. (January 2007).
1941:
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1603:
1552:
1497:
1375:
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897:
107:
50:
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structure is essential for transcription but it also requires the cluster to loop out of the
4747:
4716:
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4294:
4205:
4139:
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2323:
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2099:
Gaunt SJ (2018). "Hox cluster genes and collinearities throughout the tree of animal life".
2065:
2001:
1991:
1933:
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In 1983, the homeobox was discovered independently by researchers in two labs: Ernst Hafen,
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is necessary to specify the identity of most of the abdominal segments. A major function of
471:
is expressed along most of the abdomen, from abdominal segments 1 (A1) to A8. Expression of
204:
138:
137:
DNA sequence, the homeobox). This amino acid sequence folds into a "helix-turn-helix" (i.e.
126:
3958:
Gauchat D, Mazet F, Berney C, Schummer M, Kreger S, Pawlowski J, et al. (April 2000).
4757:
4661:
4471:
3762:"Hox C cluster genes are dispensable for overall body plan of mouse embryonic development"
1772:
Janmaat VT, Nesteruk K, Spaander MC, Verhaar AP, Yu B, Silva RA, et al. (June 2021).
1718:
1367:
1342:
1184:
1162:, has instead seen a significant loss in HOX gene clusters, with only 5 clusters present.
300:
gene is the most anteriorly expressed gene. It is expressed in the head, primarily in the
4201:
4135:
3867:
3308:
3070:
2823:
2466:
2239:
Hughes CL, Kaufman TC (2002). "Hox genes and the evolution of the arthropod body plan".
2192:
1987:
1929:
1789:
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suppress embryonic ventral epidermal structures in the eighth and ninth segments of the
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is responsible for the formation of the labial and maxillary palps. Some evidence shows
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4010:
3935:
3910:
3886:
3851:
3827:
3802:
3737:
3710:
3651:
3626:
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3383:
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3229:
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3183:
3158:
3134:
3109:
3034:
3009:
2933:
2889:
2854:
2485:
2450:
2426:
2402:"Developmental genetic analysis of Contrabithorax mutations in Drosophila melanogaster"
2401:
2377:
2352:
2319:
2006:
1971:
1888:
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1808:
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1622:
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1831:
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Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, et al. (June 2007).
2779:
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Hueber SD, Rauch J, Djordjevic MA, Gunter H, Weiller GF, Frickey T (November 2013).
2268:
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The second thoracic segment, or T2, develops a pair of legs and a pair of wings. The
4550:
4371:
4361:
4225:
4159:
4108:
3687:
3332:
3094:
2685:"p21 is a transcriptional target of HOXA10 in differentiating myelomonocytic cells"
1953:
1758:
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these genes could be traced back to patterning defects in the embryonic body plan.
1221:
1189:
1138:
1074:
903:
416:
387:
168:
63:
38:
3727:
2288:
2177:"Origin of the metazoan phyla: molecular clocks confirm paleontological estimates"
1704:
1200:, in particular, has to do with the location and layering of HOX genes within the
231:
3911:"The amphioxus genome illuminates vertebrate origins and cephalochordate biology"
2994:
2475:
2417:
2368:
1996:
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in 1980. For their work, Lewis, Nüsslein-Volhard, and
Wieschaus were awarded the
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200:
142:
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3964:
Proceedings of the
National Academy of Sciences of the United States of America
3856:
Proceedings of the
National Academy of Sciences of the United States of America
3818:
3125:
3025:
2181:
Proceedings of the National Academy of Sciences of the United States of America
2029:
Ferrier DE, Minguillón C (2003). "Evolution of the Hox/ParaHox gene clusters".
1798:
1721:(August 1995). "Homeotic genes and the evolution of arthropods and chordates".
4730:
4430:
4383:
4092:
4045:
3373:
1638:
1537:
1492:
1467:
1217:
1197:
1171:
886:
753:
180:
130:
99:
94:
3500:
Mungpakdee S, Seo HC, Angotzi AR, Dong X, Akalin A, Chourrout D (July 2008).
1878:
1447:
Discredited hypotheses for the Cambrian explosion (Section: Regulatory genes)
175:
probably had three body regions, each with a unique combination of Hox genes.
171:) by up to three segments. Segments with maxillopeds have Hox gene 7. Fossil
4681:
4649:
4416:
4322:
3876:
3558:
3518:
3501:
3424:
2831:
2612:
1265:
1245:
1142:
803:
729:
558:
211:
192:
184:
172:
164:
134:
4151:
4100:
4064:
3995:
3976:
3944:
3895:
3836:
3787:
3778:
3761:
3746:
3660:
3611:
3576:
3527:
3478:
3443:
3392:
3238:
3192:
3143:
3086:
3043:
2986:
2898:
2718:
2661:
2535:
2494:
2337:
2260:
2120:
2042:
2015:
1945:
1897:
1817:
1696:
1656:
1607:
1588:
1556:
1501:
167:. The Hox genes 7, 8, and 9 correspond in these groups but are shifted (by
4217:
3926:
3324:
3273:
2951:
2839:
2788:
2620:
2574:
2435:
2386:
2220:
2201:
2161:
2112:
2077:
1750:
411:
183:. The Hox genes, being a subset of homeobox genes, arose more recently in
179:
Homeobox genes, and thus the homeodomain protein motif, are found in most
17:
4613:
3604:
10.1002/(sici)1521-1878(200001)22:1<72::aid-bies12>3.0.co;2-s
2734:"The Origins of Anterior-Posterior Polarity: The Homeotic Selector Genes"
2152:
2135:
1338:
1326:
1322:
1311:
1295:
1229:
1225:
1134:
782:
757:
496:
492:
196:
71:
54:
34:
4143:
3174:
3078:
4376:
3695:
3470:
2978:
2700:
2451:"Improving Hox protein classification across the major model organisms"
1130:
1126:
861:
733:
725:
188:
195:(animals with a clear head-to-tail axis), and have also been found in
4356:
4209:
4175:
Master Control Genes in Development and Evolution: The Homeobox Story
3316:
1742:
1237:
1201:
1180:
1176:
1155:
1112:
1108:
1104:
1100:
1059:
1055:
1051:
1047:
1006:
949:
945:
941:
792:
721:
46:
3803:"From lizard to snake; behind the evolution of an extreme body plan"
1688:
756:
and some insects (but not most animals), Hox genes are regulated by
163:
Expression of Hox genes in the body segments of different groups of
4035:
3252:
Scott MP (November 1992). "Vertebrate homeobox gene nomenclature".
1774:"HOXA13 in etiology and oncogenic potential of Barrett's esophagus"
771:
Regulation is achieved via protein concentration gradients, called
3157:
Montavon T, Le Garrec JF, Kerszberg M, Duboule D (February 2008).
3110:"Retinoic acid synthesis and signaling during early organogenesis"
1937:
1345:
in 1894, who coined the term "homeosis". After the rediscovery of
1096:
1092:
1088:
1084:
1080:
1043:
1039:
1035:
1031:
1027:
1002:
998:
994:
990:
986:
982:
978:
974:
970:
937:
933:
929:
925:
921:
917:
913:
909:
860:
410:
230:
158:
3852:"cis-regulatory change associated with snake body plan evolution"
2400:
González-Gaitán MA, Micol JL, García-Bellido A (September 1990).
1220:, whereas there are eight HOX genes in total for the Drosophila.
1149:, have seven or eight Hox gene clusters because of an additional
4654:
1341:. Homeotic transformations were first identified and studied by
1209:
4290:
4015:
gene expression in postmetamorphic juveniles of the brachiopod
3627:"Hox genes and regional patterning of the vertebrate body plan"
3502:"Differential evolution of the 13 Atlantic salmon Hox clusters"
2134:
Lutz B, Lu HC, Eichele G, Miller D, Kaufman TC (January 1996).
2056:
Krumlauf R (July 1994). "Hox genes in vertebrate development".
2918:"Regulation of even-skipped stripe 2 in the Drosophila embryo"
2855:"Hox specificity unique roles for cofactors and collaborators"
1208:
to those of the fly as it is one of the most highly conserved
191:. Within the animal kingdom, Hox genes are present across the
89:
3211:
Lappin TR, Grier DG, Thompson A, Halliday HL (January 2006).
2302:
Regulski M, McGinnis N, Chadwick R, McGinnis W (March 1987).
1572:"Classification and nomenclature of all human homeobox genes"
374:
gene is responsible for cephalic and thoracic development in
2449:
Hueber SD, Weiller GF, Djordjevic MA, Frickey T (May 2010).
3590:
Dale KJ, Pourquié O (January 2000). "A clock-work somite".
2634:
Lohmann I, McGinnis N, Bodmer M, McGinnis W (August 2002).
1337:
The Hox genes are so named because mutations in them cause
764:, which are in their turn regulated by maternally-supplied
141:) motif that is stabilized by a third helix. The consensus
133:-long DNA-binding domain (encoded by its corresponding 180-
1244:
genes need to be knocked out in order for there to be any
680:
distal limb that will form digit, carpal and tarsal bones
106:
is the result of altered Hox coding and is a precursor to
1517:"Hox gene expression during development of the phoronid
695:
Cell cycle: differentiation of myelomonocyte cells into
3406:
Hoegg S, Boore JL, Kuehl JV, Meyer A (September 2007).
2282:
2280:
2278:
697:
monocytes (white blood cells), with cell cycle arrest
641:
boundary between the maxilla and mandible of the head
639:
Apoptosis: localized cell death creates the segmental
491:
also affects the pattern of cuticle generation in the
3213:"HOX genes: seductive science, mysterious mechanisms"
1670:
1668:
1666:
1228:. In flies, one gene can be mutated, resulting in a
876:
Mice and humans have 39 Hox genes in four clusters:
678:
Cell adhesion: causes tight association of cells in
357:
are similar to those of labial. Loss of function of
4775:
4704:
4632:
4586:
4579:
4543:
4495:
4459:
4392:
4329:
1862:"The TALE face of Hox proteins in animal evolution"
1224:are far more redundant and less likely to generate
2101:The International Journal of Developmental Biology
2031:The International Journal of Developmental Biology
1272:have a single Hox cluster with 15 genes, known as
656:prevents the above cell changes in more posterior
3206:
3204:
3202:
1570:Holland PW, Booth HA, Bruford EA (October 2007).
4240:"The Nobel Prize in Physiology or Medicine 1995"
728:. In Antennapedia, this position is occupied by
622:triggers cell shape changes in the gut that are
3625:Mallo M, Wellik DM, Deschamps J (August 2010).
2175:Ayala FJ, Rzhetsky A, Ayala FJ (January 1998).
1314:, have a few Hox/ParaHox-like homeobox genes.
818:expression domains that remain more posterior.
724:, which recognizes and binds to the nucleotide
4302:
2594:
2592:
2547:
2545:
2234:
2232:
2230:
1317:Hox gene expression has also been studied in
1288:Six Hox genes are dispersed in the genome of
844:nomenclature. The complement of Hox genes in
102:and predisposes to oncological disease, e.g.
8:
1911:
1909:
1907:
1515:Gąsiorowski L, Hejnol A (10 February 2020).
479:in insects is to repress limb formation. In
3355:Holland LZ, Ocampo Daza D (November 2018).
1838:. Department of Biosciences and Nutrition,
1409:and Amy Weiner (in Thomas Kaufman's lab at
4583:
4309:
4295:
4287:
2683:Bromleigh VC, Freedman LP (October 2000).
2351:Pattatucci AM, Kaufman TC (October 1991).
608:activates gene pathway for limb formation
594:activates gene pathway for limb formation
495:, and pattern of muscle generation in the
81:The protein product of each Hox gene is a
4054:
4044:
4034:
3985:
3975:
3934:
3885:
3875:
3826:
3777:
3736:
3726:
3676:The American Journal of Clinical Hypnosis
3650:
3566:
3517:
3433:
3423:
3382:
3372:
3228:
3182:
3133:
3033:
2941:
2888:
2778:
2708:
2651:
2525:
2484:
2474:
2425:
2376:
2327:
2210:
2200:
2151:
2005:
1995:
1887:
1877:
1807:
1797:
1646:
1597:
1587:
1546:
1536:
1491:
1204:. Vertebrates do have HOX genes that are
1179:, which form the vertebrae and ribs, the
1468:"Larval Evolution: I'll Tail You Later…"
878:
711:Enhancer sequences bound by homeodomains
624:required for normal visceral morphology
563:
2859:Current Topics in Developmental Biology
1965:
1963:
1466:Hejnol A, Vellutini BC (January 2017).
1458:
4799:Index of evolutionary biology articles
3541:Martin KJ, Holland PW (October 2014).
256:gene) consists of five genes: labial (
1384:Nobel Prize in Physiology or Medicine
7:
2740:(6th ed.). Sinauer Associates.
1621:Bürglin TR, Affolter M (June 2016).
1437:Hox genes in amphibians and reptiles
1167:Hox genes in amphibians and reptiles
813:In higher animals including humans,
3760:Suemori H, Noguchi S (April 2000).
3709:Hrycaj SM, Wellik DM (2016-05-10).
2853:Mann RS, Lelli KM, Joshi R (2009).
1137:have four HOX clusters, while most
4831:Evolutionary developmental biology
4609:Evolutionary developmental biology
2934:10.1002/j.1460-2075.1992.tb05498.x
2320:10.1002/j.1460-2075.1987.tb04819.x
779:where there is Giant and Kruppel.
235:Homeobox (Hox) gene expression in
25:
2818:(4992). New York, N.Y.: 426–430.
1623:"Homeodomain proteins: an update"
1411:Indiana University in Bloomington
4821:Developmental genes and proteins
4566:Evolution of sexual reproduction
4009:Gąsiorowski L, Hejnol A (2018).
2253:10.1046/j.1525-142x.2002.02034.x
732:, which recognizes and binds to
43:specify regions of the body plan
4081:Development Genes and Evolution
3547:Molecular Biology and Evolution
3506:Molecular Biology and Evolution
2761:Hanes SD, Brent R (June 1989).
576:Normal function of target gene
4337:Genotype–phenotype distinction
3688:10.1080/00029157.1976.10403798
523:Classification of Hox proteins
308:results in the failure of the
1:
4594:Regulation of gene expression
3728:10.12688/f1000research.7663.1
2871:10.1016/S0070-2153(09)88003-4
2653:10.1016/s0092-8674(02)00871-1
1860:Merabet S, Galliot B (2015).
1832:"Helix 1, Helix 2, Helix 3/4"
1133:from other vertebrates. Most
187:within the animal kingdom or
4764:Endless Forms Most Beautiful
4544:Evolution of genetic systems
4352:Gene–environment correlation
4347:Gene–environment interaction
3266:10.1016/0092-8674(92)90588-4
3108:Duester G (September 2008).
2780:10.1016/0092-8674(89)90063-9
2567:10.1016/0092-8674(92)90513-C
2476:10.1371/journal.pone.0010820
2070:10.1016/0092-8674(94)90290-9
1997:10.1371/journal.pone.0000153
865:Hox genes in various species
664:(represses decapentaplegic)
630:(activates decapentaplegic)
4743:Christiane Nüsslein-Volhard
4263:"The Function of Hox Genes"
3643:10.1016/j.ydbio.2010.04.024
2527:10.1016/j.ydbio.2013.09.009
2241:Evolution & Development
1372:Christiane Nüsslein-Volhard
85:. Each Hox gene contains a
4847:
4619:Hedgehog signaling pathway
4496:Developmental architecture
3850:Mansfield JH (June 2013).
3819:10.2174/138920212800793302
3801:Woltering JM (June 2012).
3217:The Ulster Medical Journal
3126:10.1016/j.cell.2008.09.002
3026:10.1016/j.cell.2007.05.022
2418:10.1093/genetics/126.1.139
2369:10.1093/genetics/129.2.443
1799:10.1038/s41467-021-23641-8
1164:
447:loss-of-function mutants,
427:
385:
129:. The homeodomain is a 60-
74:do not express Hox genes.
70:and the pilidium larva of
68:Schizocardium californicum
4796:
4446:Transgressive segregation
4093:10.1007/s00427-006-0119-y
4046:10.1186/s13227-018-0114-1
3711:"Hox genes and evolution"
3374:10.1186/s13059-018-1592-0
1639:10.1007/s00412-015-0543-8
1538:10.1186/s13227-020-0148-z
1493:10.1016/j.cub.2016.10.057
1123:whole genome duplications
669:
583:
565:Examples of target genes
4177:. Yale University Press.
1879:10.3389/fgene.2015.00267
1677:Nature Reviews. Genetics
1339:homeotic transformations
1252:formed. When the HOX10
1183:of the dorsal skin, the
1160:freshwater butterflyfish
613:(represses distal-less)
599:(represses distal-less)
4624:Notch signaling pathway
4599:Gene regulatory network
4482:Dual inheritance theory
4017:Terebratalia transversa
3877:10.1073/pnas.1307778110
3425:10.1186/1471-2164-8-317
3163:Genes & Development
2832:10.1126/science.1671176
2689:Genes & Development
2613:10.1242/dev.125.24.4949
2140:Genes & Development
1216:(A–D) on four separate
797:Polycomb-group proteins
748:Regulation of Hox genes
244:Drosophila melanogaster
237:Drosophila melanogaster
4672:cis-regulatory element
4580:Control of development
4460:Non-genetic influences
4426:evolutionary landscape
4265:. In Bittar EE (ed.).
3977:10.1073/pnas.97.9.4493
3779:10.1006/dbio.2000.9651
1589:10.1186/1741-7007-5-47
1307:Nematostella vectensis
1291:Caenorhabditis elegans
1270:Branchiostoma floridae
866:
561:, and cell migration.
420:
400:mutation, caused by a
268:), sex combs reduced (
239:
176:
39:group of related genes
4783:Nature versus nurture
4687:Cell surface receptor
4604:Evo-devo gene toolkit
4503:Developmental biology
4441:Polygenic inheritance
4367:Quantitative genetics
4267:Developmental Biology
3927:10.1101/gr.073676.107
3766:Developmental Biology
3631:Developmental Biology
3559:10.1093/molbev/msu202
3519:10.1093/molbev/msn097
2738:Developmental Biology
2514:Developmental Biology
2289:"The Interactive Fly"
2202:10.1073/pnas.95.2.606
2113:10.1387/ijdb.180162sg
1866:Frontiers in Genetics
1778:Nature Communications
1310:, both in the phylum
864:
414:
402:chromosomal inversion
272:), and Antennapedia (
234:
162:
4692:Transcription factor
4407:Genetic assimilation
4394:Genetic architecture
2153:10.1101/gad.10.2.176
1840:Karolinska Institute
808:chromosome territory
216:last common ancestor
83:transcription factor
4788:Morphogenetic field
4705:Influential figures
4202:1980Natur.287..795N
4173:Gehring WJ (1998).
4144:10.1038/nature01872
4136:2003Natur.424.1061L
4130:(6952): 1061–1065.
3868:2013PNAS..11010473M
3862:(26): 10473–10474.
3309:1994Natur.370..563G
3175:10.1101/gad.1631708
3079:10.1038/nature05916
3071:2007Natur.447..413F
2824:1991Sci...251..426H
2732:Gilbert SF (2000).
2467:2010PLoSO...510820H
2193:1998PNAS...95..606J
1988:2007PLoSO...2..153R
1930:1999Natur.399..772D
1790:2021NatCo..12.3354J
1735:1995Natur.376..479C
1519:Phoronopsis harmeri
1484:2017CBio...27..R21H
1405:, Switzerland) and
1403:University of Basel
1284:Other invertebrates
703:(activates Cdkn1a)
647:(activates reaper)
566:
302:intercalary segment
284:) and abdominal-B (
104:Barrett's esophagus
4477:Genomic imprinting
3471:10.1038/ng0606-601
2979:10.1002/bies.20704
2912:Small S, Blair A,
2701:10.1101/gad.817100
2107:(11–12): 673–683.
1354:Thomas Hunt Morgan
1325:, and a suite of
1234:adaptive radiation
1151:genome duplication
867:
773:morphogenic fields
686:(activates EphA7)
564:
421:
415:Wild type (left),
378:embryo and adult.
260:), proboscipedia (
240:
212:bilaterian animals
177:
4805:
4804:
4738:Eric F. Wieschaus
4700:
4699:
4518:Pattern formation
4422:Fitness landscape
4276:978-1-55938-816-0
4196:(5785): 795–801.
3553:(10): 2592–2611.
3303:(6490): 563–566.
3065:(7143): 413–417.
2928:(11): 4047–4057.
2916:(November 1992).
2880:978-0-12-374529-3
2695:(20): 2581–2586.
2607:(24): 4949–4957.
1924:(6738): 772–776.
1729:(6540): 479–485.
1376:Eric F. Wieschaus
1119:
1118:
708:
707:
366:Sex combs reduced
108:esophageal cancer
16:(Redirected from
4838:
4748:William McGinnis
4717:Richard Lewontin
4712:C. H. Waddington
4584:
4561:Neutral networks
4311:
4304:
4297:
4288:
4280:
4248:
4247:
4236:
4230:
4229:
4210:10.1038/287795a0
4185:
4179:
4178:
4170:
4164:
4163:
4119:
4113:
4112:
4075:
4069:
4068:
4058:
4048:
4038:
4006:
4000:
3999:
3989:
3979:
3970:(9): 4493–4498.
3955:
3949:
3948:
3938:
3921:(7): 1100–1111.
3906:
3900:
3899:
3889:
3879:
3847:
3841:
3840:
3830:
3807:Current Genomics
3798:
3792:
3791:
3781:
3757:
3751:
3750:
3740:
3730:
3706:
3700:
3699:
3671:
3665:
3664:
3654:
3622:
3616:
3615:
3587:
3581:
3580:
3570:
3538:
3532:
3531:
3521:
3512:(7): 1333–1343.
3497:
3491:
3490:
3454:
3448:
3447:
3437:
3427:
3403:
3397:
3396:
3386:
3376:
3352:
3346:
3343:
3337:
3336:
3317:10.1038/370563a0
3292:
3286:
3285:
3249:
3243:
3242:
3232:
3208:
3197:
3196:
3186:
3154:
3148:
3147:
3137:
3105:
3099:
3098:
3054:
3048:
3047:
3037:
3020:(7): 1311–1323.
3005:
2999:
2998:
2962:
2956:
2955:
2945:
2922:The EMBO Journal
2909:
2903:
2902:
2892:
2850:
2844:
2843:
2807:
2801:
2800:
2782:
2758:
2752:
2751:
2729:
2723:
2722:
2712:
2680:
2674:
2673:
2655:
2631:
2625:
2624:
2596:
2587:
2586:
2549:
2540:
2539:
2529:
2505:
2499:
2498:
2488:
2478:
2446:
2440:
2439:
2429:
2397:
2391:
2390:
2380:
2348:
2342:
2341:
2331:
2308:The EMBO Journal
2299:
2293:
2292:
2287:Brody T (1996).
2284:
2273:
2272:
2236:
2225:
2224:
2214:
2204:
2172:
2166:
2165:
2155:
2131:
2125:
2124:
2096:
2090:
2089:
2053:
2047:
2046:
2037:(7–8): 605–611.
2026:
2020:
2019:
2009:
1999:
1967:
1958:
1957:
1913:
1902:
1901:
1891:
1881:
1857:
1851:
1850:
1848:
1846:
1828:
1822:
1821:
1811:
1801:
1769:
1763:
1762:
1743:10.1038/376479a0
1715:
1709:
1708:
1672:
1661:
1660:
1650:
1618:
1612:
1611:
1601:
1591:
1567:
1561:
1560:
1550:
1540:
1512:
1506:
1505:
1495:
1463:
1407:Matthew P. Scott
1395:William McGinnis
1185:skeletal muscles
879:
857:In other species
653:decapentaplegic
619:decapentaplegic
567:
280:), abdominal-A (
139:homeodomain fold
53:of animals. Hox
21:
4846:
4845:
4841:
4840:
4839:
4837:
4836:
4835:
4811:
4810:
4808:
4806:
4801:
4792:
4771:
4758:Sean B. Carroll
4696:
4628:
4575:
4539:
4491:
4472:Maternal effect
4455:
4388:
4325:
4315:
4277:
4261:Hunt P (1998).
4260:
4257:
4255:Further reading
4252:
4251:
4238:
4237:
4233:
4187:
4186:
4182:
4172:
4171:
4167:
4121:
4120:
4116:
4077:
4076:
4072:
4008:
4007:
4003:
3957:
3956:
3952:
3915:Genome Research
3908:
3907:
3903:
3849:
3848:
3844:
3800:
3799:
3795:
3759:
3758:
3754:
3708:
3707:
3703:
3673:
3672:
3668:
3624:
3623:
3619:
3589:
3588:
3584:
3540:
3539:
3535:
3499:
3498:
3494:
3459:Nature Genetics
3456:
3455:
3451:
3405:
3404:
3400:
3354:
3353:
3349:
3344:
3340:
3294:
3293:
3289:
3251:
3250:
3246:
3210:
3209:
3200:
3156:
3155:
3151:
3107:
3106:
3102:
3056:
3055:
3051:
3007:
3006:
3002:
2964:
2963:
2959:
2911:
2910:
2906:
2881:
2852:
2851:
2847:
2809:
2808:
2804:
2760:
2759:
2755:
2748:
2731:
2730:
2726:
2682:
2681:
2677:
2633:
2632:
2628:
2598:
2597:
2590:
2551:
2550:
2543:
2507:
2506:
2502:
2448:
2447:
2443:
2399:
2398:
2394:
2350:
2349:
2345:
2301:
2300:
2296:
2286:
2285:
2276:
2238:
2237:
2228:
2174:
2173:
2169:
2133:
2132:
2128:
2098:
2097:
2093:
2055:
2054:
2050:
2028:
2027:
2023:
1969:
1968:
1961:
1915:
1914:
1905:
1859:
1858:
1854:
1844:
1842:
1830:
1829:
1825:
1771:
1770:
1766:
1717:
1716:
1712:
1689:10.1038/nrg1726
1683:(12): 893–904.
1674:
1673:
1664:
1620:
1619:
1615:
1569:
1568:
1564:
1514:
1513:
1509:
1472:Current Biology
1465:
1464:
1460:
1455:
1428:
1419:
1380:D. melanogaster
1343:William Bateson
1335:
1286:
1263:
1169:
872:
859:
839:
828:
762:pair-rule genes
750:
713:
554:
552:Regulated genes
525:
505:
461:
432:
426:
390:
384:
368:
347:
337:interacts with
324:
294:
227:
155:
150:
116:
28:
23:
22:
15:
12:
11:
5:
4844:
4842:
4834:
4833:
4828:
4823:
4813:
4812:
4803:
4802:
4797:
4794:
4793:
4791:
4790:
4785:
4779:
4777:
4773:
4772:
4770:
4769:
4768:
4767:
4755:
4750:
4745:
4740:
4735:
4734:
4733:
4722:François Jacob
4719:
4714:
4708:
4706:
4702:
4701:
4698:
4697:
4695:
4694:
4689:
4684:
4679:
4674:
4669:
4664:
4659:
4658:
4657:
4647:
4642:
4636:
4634:
4630:
4629:
4627:
4626:
4621:
4616:
4611:
4606:
4601:
4596:
4590:
4588:
4581:
4577:
4576:
4574:
4573:
4568:
4563:
4558:
4553:
4547:
4545:
4541:
4540:
4538:
4537:
4532:
4527:
4522:
4521:
4520:
4515:
4505:
4499:
4497:
4493:
4492:
4490:
4489:
4484:
4479:
4474:
4469:
4463:
4461:
4457:
4456:
4454:
4453:
4451:Sequence space
4448:
4443:
4438:
4433:
4428:
4419:
4414:
4409:
4404:
4398:
4396:
4390:
4389:
4387:
4386:
4381:
4380:
4379:
4369:
4364:
4359:
4354:
4349:
4344:
4339:
4333:
4331:
4327:
4326:
4316:
4314:
4313:
4306:
4299:
4291:
4285:
4284:
4281:
4275:
4256:
4253:
4250:
4249:
4244:Nobelprize.org
4231:
4180:
4165:
4114:
4070:
4036:10.1101/449488
4001:
3950:
3901:
3842:
3813:(4): 289–299.
3793:
3772:(2): 333–342.
3752:
3701:
3682:(3): 200–203.
3666:
3617:
3582:
3533:
3492:
3465:(6): 601–602.
3449:
3398:
3361:Genome Biology
3347:
3338:
3287:
3260:(4): 551–553.
3244:
3198:
3169:(3): 346–359.
3149:
3120:(6): 921–931.
3100:
3049:
3000:
2973:(2): 110–121.
2957:
2904:
2879:
2845:
2802:
2773:(7): 1275–83.
2753:
2746:
2724:
2675:
2646:(4): 457–466.
2626:
2588:
2561:(3): 437–450.
2541:
2520:(2): 175–185.
2500:
2441:
2412:(1): 139–155.
2392:
2363:(2): 443–461.
2343:
2314:(3): 767–777.
2294:
2274:
2247:(6): 459–499.
2226:
2187:(2): 606–611.
2167:
2146:(2): 176–184.
2126:
2091:
2064:(2): 191–201.
2048:
2021:
1959:
1903:
1852:
1823:
1764:
1710:
1662:
1633:(3): 497–521.
1613:
1562:
1507:
1478:(1): R21–R24.
1457:
1456:
1454:
1451:
1450:
1449:
1444:
1439:
1434:
1427:
1424:
1418:
1415:
1401:'s lab at the
1399:Walter Gehring
1391:Michael Levine
1334:
1331:
1285:
1282:
1262:
1259:
1240:. All of the
1165:Main article:
1117:
1116:
1077:
1072:
1064:
1063:
1024:
1019:
1011:
1010:
967:
962:
954:
953:
906:
901:
893:
892:
889:
883:
871:
868:
858:
855:
838:
835:
827:
824:
789:Non-coding RNA
749:
746:
712:
709:
706:
705:
699:
693:
689:
688:
682:
676:
673:
667:
666:
660:
654:
650:
649:
643:
637:
633:
632:
628:ULTRABITHORAX
626:
620:
616:
615:
609:
606:
602:
601:
597:ULTRABITHORAX
595:
592:
589:
581:
580:
577:
574:
571:
553:
550:
524:
521:
504:
501:
460:
457:
428:Main article:
425:
422:
419:mutant (right)
386:Main article:
383:
380:
367:
364:
346:
343:
323:
320:
293:
290:
226:
220:
154:
151:
147:
115:
112:
87:well-conserved
51:head-tail axis
35:homeobox genes
33:, a subset of
27:Group of genes
26:
24:
14:
13:
10:
9:
6:
4:
3:
2:
4843:
4832:
4829:
4827:
4826:Gene clusters
4824:
4822:
4819:
4818:
4816:
4809:
4800:
4795:
4789:
4786:
4784:
4781:
4780:
4778:
4774:
4766:
4765:
4761:
4760:
4759:
4756:
4754:
4751:
4749:
4746:
4744:
4741:
4739:
4736:
4732:
4729:
4728:
4727:
4726:Jacques Monod
4723:
4720:
4718:
4715:
4713:
4710:
4709:
4707:
4703:
4693:
4690:
4688:
4685:
4683:
4680:
4678:
4675:
4673:
4670:
4668:
4665:
4663:
4660:
4656:
4653:
4652:
4651:
4648:
4646:
4643:
4641:
4640:Homeotic gene
4638:
4637:
4635:
4631:
4625:
4622:
4620:
4617:
4615:
4612:
4610:
4607:
4605:
4602:
4600:
4597:
4595:
4592:
4591:
4589:
4585:
4582:
4578:
4572:
4569:
4567:
4564:
4562:
4559:
4557:
4554:
4552:
4549:
4548:
4546:
4542:
4536:
4533:
4531:
4528:
4526:
4523:
4519:
4516:
4514:
4511:
4510:
4509:
4508:Morphogenesis
4506:
4504:
4501:
4500:
4498:
4494:
4488:
4485:
4483:
4480:
4478:
4475:
4473:
4470:
4468:
4465:
4464:
4462:
4458:
4452:
4449:
4447:
4444:
4442:
4439:
4437:
4434:
4432:
4429:
4427:
4423:
4420:
4418:
4415:
4413:
4410:
4408:
4405:
4403:
4400:
4399:
4397:
4395:
4391:
4385:
4382:
4378:
4375:
4374:
4373:
4370:
4368:
4365:
4363:
4360:
4358:
4355:
4353:
4350:
4348:
4345:
4343:
4342:Reaction norm
4340:
4338:
4335:
4334:
4332:
4328:
4324:
4320:
4312:
4307:
4305:
4300:
4298:
4293:
4292:
4289:
4282:
4278:
4272:
4268:
4264:
4259:
4258:
4254:
4245:
4241:
4235:
4232:
4227:
4223:
4219:
4215:
4211:
4207:
4203:
4199:
4195:
4191:
4184:
4181:
4176:
4169:
4166:
4161:
4157:
4153:
4149:
4145:
4141:
4137:
4133:
4129:
4125:
4118:
4115:
4110:
4106:
4102:
4098:
4094:
4090:
4086:
4082:
4074:
4071:
4066:
4062:
4057:
4052:
4047:
4042:
4037:
4032:
4028:
4024:
4020:
4018:
4014:
4005:
4002:
3997:
3993:
3988:
3983:
3978:
3973:
3969:
3965:
3961:
3954:
3951:
3946:
3942:
3937:
3932:
3928:
3924:
3920:
3916:
3912:
3905:
3902:
3897:
3893:
3888:
3883:
3878:
3873:
3869:
3865:
3861:
3857:
3853:
3846:
3843:
3838:
3834:
3829:
3824:
3820:
3816:
3812:
3808:
3804:
3797:
3794:
3789:
3785:
3780:
3775:
3771:
3767:
3763:
3756:
3753:
3748:
3744:
3739:
3734:
3729:
3724:
3720:
3716:
3715:F1000Research
3712:
3705:
3702:
3697:
3693:
3689:
3685:
3681:
3677:
3670:
3667:
3662:
3658:
3653:
3648:
3644:
3640:
3636:
3632:
3628:
3621:
3618:
3613:
3609:
3605:
3601:
3597:
3593:
3586:
3583:
3578:
3574:
3569:
3564:
3560:
3556:
3552:
3548:
3544:
3537:
3534:
3529:
3525:
3520:
3515:
3511:
3507:
3503:
3496:
3493:
3488:
3484:
3480:
3476:
3472:
3468:
3464:
3460:
3453:
3450:
3445:
3441:
3436:
3431:
3426:
3421:
3417:
3413:
3409:
3402:
3399:
3394:
3390:
3385:
3380:
3375:
3370:
3366:
3362:
3358:
3351:
3348:
3342:
3339:
3334:
3330:
3326:
3322:
3318:
3314:
3310:
3306:
3302:
3298:
3291:
3288:
3283:
3279:
3275:
3271:
3267:
3263:
3259:
3255:
3248:
3245:
3240:
3236:
3231:
3226:
3222:
3218:
3214:
3207:
3205:
3203:
3199:
3194:
3190:
3185:
3180:
3176:
3172:
3168:
3164:
3160:
3153:
3150:
3145:
3141:
3136:
3131:
3127:
3123:
3119:
3115:
3111:
3104:
3101:
3096:
3092:
3088:
3084:
3080:
3076:
3072:
3068:
3064:
3060:
3053:
3050:
3045:
3041:
3036:
3031:
3027:
3023:
3019:
3015:
3011:
3004:
3001:
2996:
2992:
2988:
2984:
2980:
2976:
2972:
2968:
2961:
2958:
2953:
2949:
2944:
2939:
2935:
2931:
2927:
2923:
2919:
2915:
2908:
2905:
2900:
2896:
2891:
2886:
2882:
2876:
2872:
2868:
2864:
2860:
2856:
2849:
2846:
2841:
2837:
2833:
2829:
2825:
2821:
2817:
2813:
2806:
2803:
2798:
2794:
2790:
2786:
2781:
2776:
2772:
2768:
2764:
2757:
2754:
2749:
2747:0-87893-243-7
2743:
2739:
2735:
2728:
2725:
2720:
2716:
2711:
2706:
2702:
2698:
2694:
2690:
2686:
2679:
2676:
2671:
2667:
2663:
2659:
2654:
2649:
2645:
2641:
2637:
2630:
2627:
2622:
2618:
2614:
2610:
2606:
2602:
2595:
2593:
2589:
2584:
2580:
2576:
2572:
2568:
2564:
2560:
2556:
2548:
2546:
2542:
2537:
2533:
2528:
2523:
2519:
2515:
2511:
2504:
2501:
2496:
2492:
2487:
2482:
2477:
2472:
2468:
2464:
2461:(5): e10820.
2460:
2456:
2452:
2445:
2442:
2437:
2433:
2428:
2423:
2419:
2415:
2411:
2407:
2403:
2396:
2393:
2388:
2384:
2379:
2374:
2370:
2366:
2362:
2358:
2354:
2347:
2344:
2339:
2335:
2330:
2325:
2321:
2317:
2313:
2309:
2305:
2298:
2295:
2290:
2283:
2281:
2279:
2275:
2270:
2266:
2262:
2258:
2254:
2250:
2246:
2242:
2235:
2233:
2231:
2227:
2222:
2218:
2213:
2208:
2203:
2198:
2194:
2190:
2186:
2182:
2178:
2171:
2168:
2163:
2159:
2154:
2149:
2145:
2141:
2137:
2130:
2127:
2122:
2118:
2114:
2110:
2106:
2102:
2095:
2092:
2087:
2083:
2079:
2075:
2071:
2067:
2063:
2059:
2052:
2049:
2044:
2040:
2036:
2032:
2025:
2022:
2017:
2013:
2008:
2003:
1998:
1993:
1989:
1985:
1981:
1977:
1973:
1966:
1964:
1960:
1955:
1951:
1947:
1943:
1939:
1938:10.1038/21631
1935:
1931:
1927:
1923:
1919:
1912:
1910:
1908:
1904:
1899:
1895:
1890:
1885:
1880:
1875:
1871:
1867:
1863:
1856:
1853:
1841:
1837:
1833:
1827:
1824:
1819:
1815:
1810:
1805:
1800:
1795:
1791:
1787:
1783:
1779:
1775:
1768:
1765:
1760:
1756:
1752:
1748:
1744:
1740:
1736:
1732:
1728:
1724:
1720:
1714:
1711:
1706:
1702:
1698:
1694:
1690:
1686:
1682:
1678:
1671:
1669:
1667:
1663:
1658:
1654:
1649:
1644:
1640:
1636:
1632:
1628:
1624:
1617:
1614:
1609:
1605:
1600:
1595:
1590:
1585:
1581:
1577:
1573:
1566:
1563:
1558:
1554:
1549:
1544:
1539:
1534:
1530:
1526:
1522:
1520:
1511:
1508:
1503:
1499:
1494:
1489:
1485:
1481:
1477:
1473:
1469:
1462:
1459:
1452:
1448:
1445:
1443:
1442:Morphogenesis
1440:
1438:
1435:
1433:
1432:Homeotic gene
1430:
1429:
1425:
1423:
1416:
1414:
1412:
1408:
1404:
1400:
1396:
1392:
1387:
1385:
1381:
1377:
1373:
1369:
1365:
1361:
1359:
1355:
1350:
1348:
1344:
1340:
1332:
1330:
1328:
1324:
1320:
1315:
1313:
1309:
1308:
1303:
1302:
1297:
1293:
1292:
1283:
1281:
1279:
1275:
1271:
1267:
1260:
1258:
1255:
1249:
1247:
1243:
1239:
1235:
1231:
1227:
1223:
1219:
1215:
1211:
1207:
1203:
1199:
1193:
1191:
1190:invertebrates
1186:
1182:
1178:
1173:
1168:
1163:
1161:
1157:
1152:
1148:
1144:
1140:
1136:
1132:
1128:
1124:
1115:
1114:
1110:
1106:
1102:
1098:
1094:
1090:
1086:
1082:
1078:
1076:
1073:
1071:
1070:
1066:
1065:
1062:
1061:
1057:
1053:
1049:
1045:
1041:
1037:
1033:
1029:
1025:
1023:
1022:chromosome 12
1020:
1018:
1017:
1013:
1012:
1009:
1008:
1004:
1000:
996:
992:
988:
984:
980:
976:
972:
968:
966:
965:chromosome 17
963:
961:
960:
956:
955:
952:
951:
947:
943:
939:
935:
931:
927:
923:
919:
915:
911:
907:
905:
902:
900:
899:
895:
894:
890:
888:
884:
881:
880:
877:
874:
869:
863:
856:
854:
852:
847:
841:
836:
834:
830:
825:
823:
819:
816:
815:retinoic acid
811:
809:
805:
800:
798:
794:
790:
786:
784:
780:
778:
774:
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4525:Segmentation
4402:Canalisation
4372:Heterochrony
4362:Heritability
4330:Key concepts
4269:. Elsevier.
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1139:teleost fish
1120:
1079:
1075:chromosome 2
1067:
1026:
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904:chromosome 7
896:
875:
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850:
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837:Nomenclature
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829:
820:
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801:
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781:
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770:
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738:
714:
702:
696:
685:
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657:
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612:
611:ABDOMINAL-A
605:distal-less
598:
591:distal-less
585:
584:
573:Target gene
555:
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537:
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526:
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488:
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464:
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417:Antennapedia
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388:Antennapedia
382:Antennapedia
375:
371:
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358:
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350:
348:
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242:
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223:
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201:sea anemones
178:
169:heterochrony
156:
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64:hemichordate
60:
30:
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4753:Mike Levine
4662:Distal-less
4487:Polyphenism
4467:Epigenetics
4319:development
3637:(1): 7–15.
2601:Development
1982:(1): e153.
1784:(1): 3354.
1576:BMC Biology
1319:brachiopods
1218:chromosomes
1214:gene arrays
870:Vertebrates
826:Colinearity
503:Abdominal-B
459:Abdominal-A
205:duplication
143:polypeptide
127:homeodomain
4815:Categories
4731:Lac operon
4556:Robustness
4535:Modularity
4530:Metamerism
4436:Plasticity
4431:Pleiotropy
4384:Heterotopy
3418:(1): 317.
3367:(1): 209.
2865:: 63–101.
1719:Carroll SB
1627:Chromosoma
1453:References
1278:AmphiHox15
1246:phenotypic
1242:paralogous
1206:homologous
1198:drosophila
1172:Vertebrate
887:Chromosome
851:Drosophila
846:Drosophila
754:Drosophila
658:positions
586:Drosophila
517:Drosophila
489:abd-A gene
465:Drosophila
376:Drosophila
310:Drosophila
250:Drosophila
224:Drosophila
181:eukaryotes
173:trilobites
131:amino-acid
100:metaplasia
95:chromosome
49:along the
18:Hox (gene)
4682:Morphogen
4667:Engrailed
4650:Pax genes
4571:Tinkering
4417:Epistasis
4412:Dominance
4323:phenotype
3592:BioEssays
2967:BioEssays
1836:csb.ki.se
1386:in 1995.
1296:roundworm
1274:AmphiHox1
1266:Amphioxus
1261:Amphioxus
1226:mutations
1143:zebrafish
1135:tetrapods
804:chromatin
758:gap genes
730:glutamine
645:DEFORMED
570:Organism
559:apoptosis
534:Antp, Ubx
404:, causes
193:bilateria
185:evolution
165:arthropod
153:Evolution
135:base-pair
122:enhancers
31:Hox genes
4645:Hox gene
4633:Elements
4614:Homeobox
4152:12944969
4101:17180685
4065:30637095
3996:10781050
3945:18562680
3896:23749870
3837:23204918
3788:10753520
3747:27239281
3661:20435029
3612:10649293
3577:24974377
3528:18424774
3487:41211603
3479:16736008
3444:17845724
3393:30486862
3282:13370372
3239:16457401
3193:18245448
3144:18805086
3087:17522674
3044:17604720
2987:18200528
2914:Levine M
2899:19651302
2797:22478337
2719:11040212
2670:17464919
2662:12202035
2583:10977579
2536:24055174
2495:20520839
2455:PLOS ONE
2406:Genetics
2357:Genetics
2338:16453752
2269:46085797
2261:12492146
2121:30604837
2086:39168197
2043:14756336
2016:17252055
1976:PLOS ONE
1946:10391241
1898:26347770
1845:March 9,
1818:34099670
1697:16341070
1657:26464018
1608:17963489
1557:32064072
1531:(2): 2.
1502:28073016
1426:See also
1417:Research
1368:Ed Lewis
1327:molluscs
1323:annelids
1312:Cnidaria
1268:such as
1254:paralogs
1222:Clusters
1127:lampreys
799:(PRC2).
783:MicroRNA
701:Hox-A10
684:HOX-A13
497:mesoderm
493:ectoderm
345:Deformed
210:In most
199:such as
197:Cnidaria
114:Function
72:Nemertea
66:species
55:proteins
37:, are a
4776:Debates
4587:Systems
4513:Eyespot
4377:Neoteny
4226:4337658
4218:6776413
4198:Bibcode
4160:4317828
4132:Bibcode
4109:7314266
4056:6325747
4031:bioRxiv
4023:EvoDevo
3936:2493399
3887:3696806
3864:Bibcode
3828:3394116
3738:4863668
3721:: 859.
3652:2909379
3568:4166920
3435:2080641
3384:6260733
3333:4329696
3325:7914353
3305:Bibcode
3274:1358459
3230:1891803
3184:2216694
3135:2632951
3095:4388060
3067:Bibcode
3035:2084369
2952:1327756
2890:2810641
2840:1671176
2820:Bibcode
2812:Science
2789:2500253
2621:9811579
2575:1358457
2486:2876039
2463:Bibcode
2436:1977655
2427:1204118
2387:1683847
2378:1204635
2221:9435239
2189:Bibcode
2162:8566751
2078:7913880
2007:1779807
1984:Bibcode
1954:4413694
1926:Bibcode
1889:4539518
1872:: 267.
1809:8184780
1786:Bibcode
1759:4230019
1751:7637779
1731:Bibcode
1648:4901127
1599:2211742
1548:7011278
1525:EvoDevo
1480:Bibcode
1333:History
1230:haltere
1177:somites
1131:hagfish
882:Cluster
734:adenine
726:guanine
692:Cdkn1a
636:reaper
189:Metazoa
4677:Ligand
4357:Operon
4273:
4224:
4216:
4190:Nature
4158:
4150:
4124:Nature
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1918:Nature
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1655:
1645:
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1555:
1545:
1500:
1393:, and
1347:Mendel
1202:genome
1181:dermis
1156:salmon
1147:medaka
1113:HOXD13
1109:HOXD12
1105:HOXD11
1101:HOXD10
1060:HOXC13
1056:HOXC12
1052:HOXC11
1048:HOXC10
1007:HOXB13
950:HOXA13
946:HOXA11
942:HOXA10
891:Genes
885:Human
793:HOTAIR
722:lysine
675:EphA7
530:Hox6-8
292:Labial
47:embryo
45:of an
4283:Fatim
4222:S2CID
4156:S2CID
4105:S2CID
4029:: 1.
3987:18262
3483:S2CID
3329:S2CID
3278:S2CID
3091:S2CID
2995:53138
2991:S2CID
2793:S2CID
2666:S2CID
2579:S2CID
2265:S2CID
2212:18467
2082:S2CID
1950:S2CID
1755:S2CID
1701:S2CID
1301:Hydra
1238:phyla
1210:genes
1097:HOXD9
1093:HOXD8
1089:HOXD4
1085:HOXD3
1081:HOXD1
1069:HOXD@
1044:HOXC9
1040:HOXC8
1036:HOXC6
1032:HOXC5
1028:HOXC4
1016:HOXC@
1003:HOXB9
999:HOXB8
995:HOXB7
991:HOXB6
987:HOXB5
983:HOXB4
979:HOXB3
975:HOXB2
971:HOXB1
959:HOXB@
938:HOXA9
934:HOXA7
930:HOXA6
926:HOXA5
922:HOXA4
918:HOXA3
914:HOXA2
910:HOXA1
898:HOXA@
671:Mouse
538:abd-A
513:abd-B
509:abd-B
507:Gene
485:abd-A
481:abd-A
477:abd-A
473:abd-A
469:abd-A
286:abd-B
282:abd-A
41:that
4317:The
4271:ISBN
4214:PMID
4148:PMID
4097:PMID
4061:PMID
3992:PMID
3941:PMID
3892:PMID
3833:PMID
3784:PMID
3743:PMID
3696:2005
3692:PMID
3657:PMID
3608:PMID
3573:PMID
3524:PMID
3475:PMID
3440:PMID
3389:PMID
3321:PMID
3270:PMID
3254:Cell
3235:PMID
3189:PMID
3140:PMID
3114:Cell
3083:PMID
3040:PMID
3014:Cell
2983:PMID
2948:PMID
2895:PMID
2875:ISBN
2836:PMID
2785:PMID
2767:Cell
2742:ISBN
2715:PMID
2658:PMID
2640:Cell
2617:PMID
2571:PMID
2555:Cell
2532:PMID
2491:PMID
2432:PMID
2383:PMID
2334:PMID
2257:PMID
2217:PMID
2158:PMID
2117:PMID
2074:PMID
2058:Cell
2039:PMID
2012:PMID
1942:PMID
1894:PMID
1847:2022
1814:PMID
1747:PMID
1693:PMID
1653:PMID
1604:PMID
1553:PMID
1498:PMID
1397:(in
1374:and
1304:and
1294:, a
1145:and
1129:and
802:The
766:mRNA
760:and
546:Antp
544:and
542:Hox7
532:and
406:Antp
398:Antp
394:Antp
370:The
349:The
331:gene
326:The
296:The
274:Antp
254:Antp
4321:of
4206:doi
4194:287
4140:doi
4128:424
4089:doi
4085:217
4051:PMC
4041:doi
4013:Hox
3982:PMC
3972:doi
3931:PMC
3923:doi
3882:PMC
3872:doi
3860:110
3823:PMC
3815:doi
3774:doi
3770:220
3733:PMC
3723:doi
3684:doi
3647:PMC
3639:doi
3635:344
3600:doi
3563:PMC
3555:doi
3514:doi
3467:doi
3430:PMC
3420:doi
3379:PMC
3369:doi
3313:doi
3301:370
3262:doi
3225:PMC
3179:PMC
3171:doi
3130:PMC
3122:doi
3118:134
3075:doi
3063:447
3030:PMC
3022:doi
3018:129
2975:doi
2938:PMC
2930:doi
2885:PMC
2867:doi
2828:doi
2816:251
2775:doi
2705:PMC
2697:doi
2648:doi
2644:110
2609:doi
2605:125
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2522:doi
2518:383
2481:PMC
2471:doi
2422:PMC
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2410:126
2373:PMC
2365:doi
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2324:PMC
2316:doi
2249:doi
2207:PMC
2197:doi
2148:doi
2109:doi
2066:doi
2002:PMC
1992:doi
1934:doi
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1276:to
777:not
536:and
463:In
453:Ubx
449:Ubx
445:Ubx
441:Ubx
436:Ubx
372:Scr
359:Dfd
355:Dfd
351:Dfd
339:Scr
315:lab
306:lab
298:lab
288:).
278:Ubx
270:Scr
266:Dfd
258:lab
222:In
90:DNA
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